Evolution of the alternate photosynthetic pathways

Both C4 and CAM pathways have evolved many times in many plant families.

C4

While there are many dicot C4 species, this pathway is most common (about ½ the species) in the grasses (Monocotyledenae; Poaceae).

There are only a few genera in which there is a mixture of C3

and C4 species, and an even rarer few that are ‘intermediate’.

Since even the best fossils don’t preserve biochemical pathways, we have only indirect evidence of the steps in evolution of the alternate pathways.

From one of the genera (Flaveria) with ‘intermediate’ photosynthesis, we can get some ideas…

1. Change in bundle sheath cells, differentiating them structurally (and later biochemically) from mesophyll. McKown (2007) believes that the evolution of the Krantz anatomy preceded the biochemical evolutionary steps to reach C4 photosynthesis.

CO2 released by photorespiration in mesophyll cells may have been ‘recycled’ in the bundle sheath using rubisco to fix it (free of the possibility of photorespiration in this tissue). Plants that ‘recycled’ would have an advantage.

2. The amount and activity of PEP carboxylase in mesophyll increased, capturing carbon with greater affinity.

The other enzymes involved in C4 fixation and conversion to the PGAL used by the Calvin-Benson pathway would then have similarly increased in abundance.

3. Separation of the functions anatomically would have followed logically. Restricting rubisco to bundle sheath cells would have eliminated photorespiration.

CAM

CAM photosynthesis is more widely dispersed among plant families than C4. It is found in very primitive vascular plants, in ferns, and in many higher plant families. It is most commonly found in epiphytes and succulent xerophytes (some photos on the next slide).

Its evolution also seems more direct, if without clear, stepwise evidence. CAM may well have evolved as a means to ‘recycle’ CO2 produced by plant respiration at night. Biochemical evolution would have followed once the temporal concentration of CO2 had occurred.

A cactus A Euphorb

Isocetes (a quillwort) A bromeliad Spanish moss

Another aspect that may have influenced the evolution of the alternate pathways is the change in the concentration of atmospheric CO2 over geological time.

Over much of the time during which plants evolved, atmospheric CO2 levels were much higher than today. In the Mesozoic, when gymnosperms dominated, partial pressures of CO2 were >1000ppm. There was little chance of photorespiration.

By the time angiosperms were radiating rapidly, CO2 partial pressures were only about 2x current levels. As CO2 decreased, the advantage of the alternative pathways increased.

Your text asks the interesting question: Is the increase in greenhouse gases reducing the advantage of C4 and CAM?

Distribution of species with alternate photosynthetic pathways

The most common CAM plants are succulents in arid environments (but not the very driest desert areas) and epiphytes in subtropical and tropical communities.

Both habitat types are relatively dry. Succulence clearly stores water for dry periods. Plants like Spanish moss and other epiphytes are dependent on capture of rainfall and mineral nutrients washing down the trunk of the tree on which they grow.

C4 plants are most common among annual plants and in prairie and steppe grasslands. Their advantage is maximized in warm climates, thus they tend to be ‘summer’ plants. Since they grow in the same places as C3s, how can they be distinguished?

Distinguishing characteristics of C4s:

1. The presence of the Krantz anatomy.

2. 13 C – C3 photosynthesis, based on carbon capture by rubisco, has a lower relative amount of the C13 isotope than the atmosphere. PEP carboxylase does not discriminate among carbon isotopes, and has a ratio of C12 to C13 essentially identical to the atmosphere. A standard means of identifying previously unrecognized C4 species is by measuring the 13 C:

13 C = [(13C/12C)sample – (13C/12C)standard] x 1000(13C/12C)standard

The ‘standard’ is the isotopic ratio for a special dolomite (CaMg(CO3)2) from the PeeDee formation (Cretaceous fossils of a marine fossil)found in N. and S. Carolina.

We can also examine the distribution of C4 species…

The advantage conferred by warm climates suggests that we would find more C4 species in the southern United States and Mexico than further north in Canada. Maps from the text indicate that:

As a generalized pattern of presence-absence across North America, your text has a curious figure to depict where C3

grasses, C4 grasses, and shrubs occur…

There is a different approach that adds some information about the history of C4 plant distribution in North American grasslands…

Because the bundle sheath of C4 plants is highly lignified and/or contains a lot of silica, the bundle sheath is tough to chew. It’s also where most of the ‘goodies’ are – fixed carbohydrate and large amounts of rubisco protein.

In the fossil beds in Kansas called “Kansan equus beds” (guess what fossils were first considered important from there?) there is a history of fossils representing the evolution of small prairie rodents, particularly microtines.

The fossils predate the arrival (or at least the increase in abundance) of C4 grasses.

The currently dominant prairie vole, Microtus ochrogaster, has molar teeth adapted to the grinding of C4 grasses to obtain the nutrients from the bundle sheath. As a keying characteristic, the molars have 5-7 closed triangles (ridges on the surface of the teeth, diagram coming up in the next slide).

The ancestors of these Microtus have, at appearance in the equus beds, only 3 closed triangles (less ability to grind), and the number increases through evolutionary time among the fossils.

Meanwhile, Microtus pennsylvanicus, a contemporary close relative that overlaps with the prairie vole, but is more centered in eastern North America, in an area much more dominated by C3 grasses, has molar teeth with the keying characteristic of 3-5 closed triangles.

M. pennsylvanicus upper molarsThe third is the keying molar, with only three closed triangles.

This is a different Microtus species (not ochrogaster) from an area with more C4 grasses.

One last adaptive character in plants is the ability to adjust leaf angle/position to maximize solar energy captured through the daily ‘solar cycle’.

There are plants in many places that are capable of ‘solar tracking’, but its importance is greatest where the solar angle makes the adaptation most valuable – at higher latitudes.

How much differencedoes solar tracking make?

Among the plants (in these species, flowers) that track the sun:

Dryas integrifolia in the arctic

Compass plant (Silphium laciniatum) from an Illinois prairie

Bibliography

McKown A.D. & Dengler N.G. (2007) Key innovations in the evolution of Kranz anatony and C4 vein pattern in Flaveria (Asteraceae). American Journal of Botany 94, 382–399.

McKown A.D.,Moncalvo J.M.&Dengler N.G. (2005) Phylogeny of Flaveria (Asteraceae) and inference of C4 photosynthesis evolution. American Journal of Botany 92, 1911–1928.